The Secret Lives of Birds

Startling new discoveries about mating behavior are revolutionizing the field of bird biology

04-01-1993
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John Carey

At first glance, the razorbill seems to be a model of bird world monogamy. Males and females rear their young on precarious cliff ledges in cozy family units. But when ornithologist Richard H. Wagner of the National Zoo in Washington, D.C., spied on these big, black and white colonial seabirds on a shore, he discovered a secret side to their mating behavior. Before laying their eggs, at least half of the females leave their mates and slip off to another ledge to copulate with other males. And later, while their mates are safely occupied incubating their eggs, the females slip away again to the ledge for more copulation.

What's particularly surprising is that these later couplings seem to have nothing to do with reproduction, since the females are no longer fertile. "Remind you of any mammal you're familiar with?" asks Stanford University biologist Paul R. Ehrlich.

Of course, questions about human behavior are better left to Freud or Dr. Ruth. But for razor bills, Wagner has an intriguing hypothesis. The whole colony returns to the same cliffside nesting sites year after year. And when they come back, "I think they remember each other," he says. As a result, the couplings "are like auditions," he speculates-females are putting the males through their paces to spot the best prospect for next year's mating.

Strange though it seems, this behavior among razorbills is only one of many startling new findings that are revolutionizing the field of bird behavior. Ornithologists once may have waxed rhapsodic about monogamous avian relationships in species like geese and Europe's crowlike jackdaws. But today, scientists increasingly are discovering that family life among the feathered set is full of unexpected surprises.

In recent years, for example, scientists discovered that older male purple martins intentionally will try to lure younger, inexperienced males to a nest site, in order to copulate with the mates the younger birds manage to attract. In Antarctica, biologists found that battles among Adelie penguins--once thought to be males fighting for territory-are really fights between females over males. "It's almost to the point where we don't know what bizarre thing will crop up next," says University of Nevada ornithologist Lewis W. Oring.

Indeed, the last few years has brought a "fantastic blossoming of studies," says Patricia Adair Gowaty of the University of Georgia, in part because of the power of molecular biology. In the late 1980s, ornithologists began to test traditional ideas about avian families using so-called DNA "fingerprinting." That made it possible for researchers to discern the true parents of each chick-and the results often were startling to scientists.

In species after species, from such supposedly monogamous birds as warblers to polygamous species like red-winged blackbirds, anywhere from 15 to 50 percent of the offspring are sired by males other than a female's own mate. In many cases, in fact, eggs in the same clutch of one female are fertilized by different males. Discovering the widespread extent of what biologists call extra-pair copulations, says Oring, "was a major breakthrough. It's forcing a conceptual reevaluation of bird breeding strategies."

Consider scientists' views of avian "adultery" (which, of course, is a value-laden term that wildlife biologists carefully avoid). Until recently, ornithologists-most of them men-regarded this phenomenon as a male-driven strategy. Mating with many females increases the chances of having many offspring. Evolution, therefore, should favor "promiscuous" males.

On the other hand, a bird that constantly flits about in search of females leaves the door open for other males to copulate with his own mate. In addition, more of his offspring might survive if he stuck around to care for them. Thus, many aspects of a species' social structure could be explained by whether males put energy into caring for (and guarding) their own mates or into copulating with more than one female.

But this male-centered perspective is being vanquished by the new research. "It is just beginning to dawn on people that females are seeking extra-pair copulations," says Richard Wagner. "They often are not being forced." As a result, many of the old ideas about monogamy in the avian kingdom recently have been shattered.

The idea of female birds actively soliciting sexual activity raises some vexing questions. For males, the risks of extra-pair copulations are small compared to the benefits of fathering more offspring, explains Cornell University biologist Paul Sherman. "But for a female," he says, "the potential costs are immense." After all, she's the one that has to shoulder the burden of producing eggs and, in most species, incubating them. So according to natural selection theory, a female cannot seek these extra-pair copulations just because she likes to mate. Ultimately, the pairings must offer her a boost in reproductive success. The question is, how? One plausible answer is the so-called avian equivalent of the human lament that "a good man is hard to find."

Biologists believe that just because a male bird is strong, a fast flier and sire to many robust chicks does not necessarily mean he also will be a model mate who spends all of his time providing for his mate and offspring. So female birds often may be striving for the best of both worlds. They can pick a mate that is an excellent provider. Yet at the same time, they can copulate with males whose seemingly superior genes have made them grow bigger, stronger or longer-lived.

Tantalizing evidence for this notion comes from studies of black-capped chickadees in Massachusetts. In these small songbirds, "pair bonds are a very important part of the social structure," explains Mount Holyoke College biologist Susan Smith. A male takes on the responsibility of feeding his mate during the 16 to 18 days that she spends incubating her eggs and brooding the young. The bond even endures through the winter. Yet in this highly monogamous species, Smith discovered, some females actually "steal out" to mate with other males. They don't, however, just pick any available males.

Chickadee society has a well-established pecking order. Older, more experienced birds are almost always dominant over younger ones. Researchers like Smith suspect that this social order doesn't arise by chance. In fact, the higher "rank" of the dominant birds could be evidence of better genes. So which males do the straying females pick to sire their young? In every case, females copulate with males ranked higher than their own mates in the chickadee pecking order, presumably getting more-fit genes for their offspring in the process.

Similarly, male red-winged blackbirds with established territories are far more successful at extra-pair copulations than are so-called "floater" males-those without their own territories. But the story isn't as neat as it first appears. The next step is for biologists to prove that the more dominant birds or higher-ranked males really do have superior genes.

When he first looked at red-winged blackbird society, says University of Pittsburgh ornithologist William Searcy, "I thought it was a meritocracy-the best males get best territories." But after examining every conceivable measure-from body size to brightness of the birds' red epaulettes-and finding no discernible difference, the scientist remains puzzled. "Now it looks like it is a random process," says Searcy.

Still, study after study is showing that female birds are making choices among these males, and biologists are determined to find out what the females are looking for. That's why researchers began the huge task of marking all the birds in a small population, sampling their DNA and observing their behavior. The goal is to identify the genetic parents of every chick and compare the real father to the mother's mate, and thereby better understand avian extra-pair copulation. "This is the frontier right now," says Paul. Sherman.

The new studies of avian sexual behavior are managing to solve some longtime conundrums. Consider the case of the seemingly inbred fairy wren. These chickadee-sized birds live on the Australian heath in extended family groups. "Initial studies had found extremely highrates of relatives-often siblings-being paired to each other," explains biologist David Westneat of the University of Kentucky. "The little birds seemed to have one of the highest rates of inbreeding known."

The rates were so high, in fact, that scientists wondered how the species avoided fatal genetic flaws. But when Australian researchers actually did conduct DNA paternity tests, they discovered that the birds were in no genetic danger. The reason: Females copulate with other males in addition to their apparent mates, and either through timing or internal biology, their eggs are fertilized by males outside the family. Thus, the fairy wren offspring are not being sired by the apparent fathers.

DNA sleuthing has also deciphered a particularly strange puzzle in the spotted sandpiper. "Their breeding system is astonishing," says Nevada's Lewis Oring, who has studied the shorebirds for nearly two decades on an island in Minnesota. "Females arrive first in the spring and set up a territory on the beach. They mate and lay eggs. But then they leave their first mate to incubate the eggs and hustle another male." In fact, females may mate with as many as four males, each of whom dutifully incubates the resulting eggs.

A female sandpiper, Oring found, is capable of performing motherly tasks. If her first male is killed, she will incubate the eggs herself. Hence the enigma. Why doesn't the first male simply skedaddle, leaving the female to nurture the eggs, thus freeing himself to father another clutch with another female? Oring's DNA analysis turned up an astonishing answer: The father of about 11 percent of the eggs in later clutches turns out to be the first male.

Like females of many other species, sandpiper females can store sperm from earlier sexual encounters. But in most birds, the sperm is viable only a short time; it usually is pushed out by sperm from later copulations. Apparently, though, sandpipers can store sperm for days and still use it even after copulating with other males. As a result, the first male doesn't have to leave his eggs to sire more chicks.

Such discoveries make bird mating behavior one of the hottest topics today in organismic biology. And as in any seething area of science, disagreements among researchers are almost as entertaining as the mating behavior of the birds themselves.

One sticky issue is why younger males in some species forgo mating in order to help older relatives rear their young. Some biologists think that the birds are biding their time, waiting for a chance to become top dog. Other experts insist that the helpers are ensuring that at least some of their genes (those shared by the young) are being passed on. Advocates of each side "get together at meetings and scream at each other," says one neutral biologist.

Sometimes, combatants line up along national boundaries. In Scandinavia, for example, the pied flycatcher has Norwegian ornithologists fighting--genteelly, of course--with Swedish scientists. In this little songbird's curious mating system, a male sets up a territory, attracts a female and starts a family. Then he does it all over again in a neighboring territory. Finally, he goes "home" and helps raise his first family, leaving his second mate to struggle with single motherhood.

So why does this second female mate with such a cad? The Swedes are convinced that she's been completely deceived--that she can't tell the male is already mated. Bosh, say the Norwegians. She can see right through the male's scheme, they argue, but males are scarce and she wants to make the best of a bad job. "It's an intense rivalry," says Pittsburgh's William Searcy, who collaborates with the Swedes.

In short, bird behavior these days is a veritable soap opera, complete with everything from wandering females to battling ornithologists. For those who prefer that Nature provide examples of more traditional views regarding. avian mating behavior, the new studies have turned up a few species-seagoing fulmars and masked boobies, for instance-that do seem to be sexually as well as socially monogamous. And there is no lack of spicy mysteries left to be solved. What do selective female red-winged blackbirds know about males that biologists haven't yet discovered? Do male razorbills get more proficient at copulation because of the species' sexual "auditions"? And why are Swedes more likely than Norwegians to believe that certain females are easily deceived? Tune in again in a few more years for the startling answers.

John Carey is a science correspondent for Business Week in Washington, D.C.